Skip to main content
Key Specialties
Cardiology Diabetology Endocrinology Gastroenterology Geriatrics and Gerontology Gynecology and Obstetrics Hematology Infectious Disease Internal Medicine Nephrology Neurology Oncology Pediatrics Respiratory Medicine Rheumatology Surgery
Congress Coverage
2024 ACC Congress 2023 ESMO Congress 2023 EASD Congress 2023 ERS Congress 2023 ESC Congress
Clinical Collections
Advances in Alzheimer’s

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.
ADVANCED SEARCH
Log in
Top
Gut Pathogens
Published in: Gut Pathogens 1/2020

Open Access 01-12-2020 | Escherichia Coli | Research

Transcriptome changes and polymyxin resistance of acid-adapted Escherichia coli O157:H7 ATCC 43889

Authors: Daekeun Hwang, Seung Min Kim, Hyun Jung Kim

Published in: Gut Pathogens | Issue 1/2020

Login to get access

Abstract

Background

Acid treatment is commonly used for controlling or killing pathogenic microorganisms on medical devices and environments; however, inadequate acid treatment may cause acid tolerance response (ATR) and offer cross-protection against environmental stresses, including antimicrobials. This study aimed to characterise an Escherichia coli strain that can survive in the acidic gastrointestinal environment.

Results

We developed an acid-tolerant E. coli O157:H7 ATCC 43889 (ATCC 43889) strain that can survive at pH 2.75 via cell adaptation in low pH conditions. We also performed RNA sequencing and qRT-PCR to compare differentially expressed transcripts between acid-adapted and non-adapted cells. Genes related to stress resistance, including kdpA and bshA were upregulated in the acid-adapted ATCC 43889 strain. Furthermore, the polymyxin resistance gene arnA was upregulated in the acid-adapted cells, and resistance against polymyxin B and colistin (polymyxin E) was observed. As polymyxins are important antibiotics, effective against multidrug-resistant gram-negative bacterial infections, the emergence of polymyxin resistance in acid-adapted E. coli is a serious public health concern.

Conclusion

The transcriptomic and phenotypic changes analysed in this study during the adaptation of E. coli to acid environments can provide useful information for developing intervention technologies and mitigating the risk associated with the emergence and spread of antimicrobial resistance.
Appendix
Available only for authorised users
Literature
1.
Wang L, Bassiri M, Najafi R, Najafi K, Yang J, Khosrovi B, et al. Hypochlorous acid as a potential wound care agent: part I. Stabilized hypochlorous acid: a component of the inorganic armamentarium of innate immunity. J Burns Wounds. 2007;6:e5.PubMedPubMedCentral
2.
Foster JW. Escherichia coli acid resistance: tales of an amateur acidophile. Nat Rev Microbiol. 2004;2:898–907.CrossRefPubMed
3.
4.
Pijuan M, Wang Q, Ye L, Yuan Z. Improving secondary sludge biodegradability using free nitrous acid treatment. Bioresour Technol. 2012;116:92–8.CrossRefPubMed
5.
Wheeler TL, Kalchayanand N, Bosilevac JM. Pre- and post-harvest interventions to reduce pathogen contamination in the U.S. beef industry. Meat Sci. 2014;98(3):372–82.CrossRefPubMed
6.
Park C-M, Hung Y-C, Doyle MP, Ezeike GOI, Kim C. Pathogen reduction and quality of lettuce treated with electrolyzed oxidizing and acidified chlorinated water. J Food Sci. 2001;66(9):1368–72.CrossRef
7.
Kanjee U, Houry WA. Mechanisms of acid resistance in Escherichia coli. Annu Rev Microbiol. 2013;67(1):65–81.CrossRefPubMed
8.
Hwang D, Kim SM, Kim HJ. Modelling of tetracycline resistance gene transfer by commensal Escherichia coli food isolates that survived in gastric fluid conditions. Int J Antimicrob Agents. 2017;49(1):81–7.CrossRefPubMed
9.
Leyer GJ, Johnson EA. Acid adaptation induces cross-protection against environmental stresses in Salmonella typhimurium. Appl Environ Microbiol. 1993;59(6):1842–7.CrossRefPubMedPubMedCentral
10.
Yousef AE, Juneja VK. Microbial stress adaptation and food safety. Boca Raton: CRC Press; 2002.CrossRef
11.
Li Y-H, Hanna MN, Svensäter G, Ellen RP, Cvitkovitch DG. Cell density modulates acid adaptation in Streptococcus mutans: implications for survival in biofilms. J Bacteriol. 2001;183(23):6875–84.CrossRefPubMedPubMedCentral
12.
Delignette-Muller ML, Rosso L. Biological variability and exposure assessment. 2000;58:203–12.
13.
Zhang W, Li F, Nie L. Integrating multiple ‘omics’ analysis for microbial biology : application and methodologies. Microbiology. 2010;156:287–301.CrossRefPubMed
14.
Cheng H-Y, Yu R-C, Chou C-C. Increased acid tolerance of Escherichia coli O157: H7 as affected by acid adaptation time and conditions of acid challenge. Food Res Int. 2003;36(1):49–56.CrossRef
15.
Berry ED, Cutter CN. Effects of acid adaptation of Escherichia coli O157:H7 on efficacy of acetic acid spray washes to decontaminate beef carcass tissue. Appl Environ Microbiol. 2000;66(4):1493–8.CrossRefPubMedPubMedCentral
16.
Reischl U, Youssef MT, Kilwinski J, Lehn N, Zhang WL, Karch H, et al. Real-time fluorescence PCR assays for detection and characterization of Shiga toxin, intimin, and enterohemolysin genes from Shiga toxin-producing Escherichia coli. J Clin Microbiol. 2002;40(7):2555–65.CrossRefPubMedPubMedCentral
17.
18.
Buchanan RL, Edelson SG. Culturing enterohemorrhagic Escherichia coli in the presence and absence of glucose as a simple means of evaluating the acid tolerance of stationary-phase cells. Appl Environ Microbiol. 1996;62(11):4009–13.CrossRefPubMedPubMedCentral
19.
Lalou S, Hatzidimitriou E, Papadopoulou M, Kontogianni VG, Tsiafoulis CG, Gerothanassis IP, et al. Beyond traditional balsamic vinegar: compositional and sensorial characteristics of industrial balsamic vinegars and regulatory requirements. J Food Compos Anal. 2015;43:175–84.CrossRef
20.
Simonian HP, Vo L, Doma S, Fisher RS. Regional postprandial differences in pH within the stomach and gastroesophageal junction. Dig Dis Sci. 2005;50(12):2276–85.CrossRefPubMed
21.
Huddleston JR. Horizontal gene transfer in the human gastrointestinal tract: potential spread of antibiotic resistance genes. Infect Drug Resist. 2014;20(7):167–76.CrossRef
22.
Rossi F, Rizzotti L, Felis GE, Torriani S. Horizontal gene transfer among microorganisms in food: current knowledge and future perspectives. Food Microbiol. 2014;42:232–43.CrossRefPubMed
23.
Peng S, Stephan R, Hummerjohann J, Tasara T. Transcriptional analysis of different stress response genes in Escherichia coli strains subjected to sodium chloride and lactic acid stress. FEMS Microbiol Lett. 2014;361(2):131–7.CrossRefPubMed
24.
Maiden MCJ, Jones-Mortimer MC, Harnett JE, Holman GI, Munday KA, Feany MH, et al. Multiple mechanisms, roles and controls of K transport in Escherichia coli. Eur J Hiochem. 1993;215:54.
25.
26.
Martirosov SM, Petrosian LS, Trchounian AA, Vartanian AG. An electrochemical study of energy-dependent potassium accumulation in E. coli: membrane potential (in comparison with that of S. faecalis). J Electroanal Chem Interfacial Electrochem. 1981;128:613–20.CrossRef
27.
Greie J-C. The KdpFABC complex from Escherichia coli: a chimeric K+ transporter merging ion pumps with ion channels. Eur J Cell Biol. 2011;90(9):705–10.CrossRefPubMed
28.
Ryan D, Pati NB, Ojha UK, Padhi C, Ray S, Jaiswal S, et al. Global transcriptome and mutagenic analyses of the acid tolerance response of Salmonella enterica serovar typhimurium. Appl Environ Microbiol. 2015;81(23):8054–65.CrossRefPubMedPubMedCentral
29.
Wang S, Deng K, Zaremba S, Deng X, Lin C, Wang Q, et al. Transcriptomic response of Escherichia coli O157:H7 to oxidative stress. Appl Environ Microbiol. 2009;75(19):6110–23.CrossRefPubMedPubMedCentral
30.
Zhang X-S, García-Contreras R, Wood TK. YcfR (BhsA) influences Escherichia coli biofilm formation through stress response and surface hydrophobicity. J Bacteriol. 2007;189(8):3051–62.CrossRefPubMedPubMedCentral
31.
Andersson DI, Hughes D. Antibiotic resistance and its cost: is it possible to reverse resistance? Nat Rev Micro. 2010;8(4):260–71.CrossRef
32.
Nuoffer C, Zanolari B, Erni B. Glucose permease of Escherichia coli. The effect of cysteine to serine mutations on the function, stability, and regulation of transport and phosphorylation. J Biol Chem. 1988;263(14):6647–55.PubMed
33.
Hua Q, Yang C, Oshima T, Mori H, Shimizu K. Analysis of gene expression in Escherichia coli in response to changes of growth-limiting nutrient in chemostat cultures. Appl Environ Microbiol. 2004;70(4):2354–66.CrossRefPubMedPubMedCentral
34.
Heyde M, Portalier R. Regulation of major outer membrane porin proteins of Escherichia coli K 12 by pH. Mol Gen Genet MGG. 1987;208(3):511–7.CrossRefPubMed
35.
Malki A, Le H-T, Milles S, Kern R, Caldas T, Abdallah J, et al. Solubilization of protein aggregates by the acid stress chaperones HdeA and HdeB. J Biol Chem. 2008;283(20):13679–87.CrossRefPubMed
36.
Stancik LM, Stancik DM, Schmidt B, Barnhart DM, Yoncheva YN, Slonczewski JL. pH-dependent expression of periplasmic proteins and amino acid catabolism in Escherichia coli. J Bacteriol. 2002;184(15):4246–58.CrossRefPubMedPubMedCentral
37.
Olier M, Rousseaux S, Piveteau P, Lemaı̂tre JP, Rousset A, Guzzo J. Screening of glutamate decarboxylase activity and bile salt resistance of human asymptomatic carriage, clinical, food, and environmental isolates of Listeria monocytogenes. Int J Food Microbiol. 2004;93(1):87–99.CrossRefPubMed
38.
Castanie-Cornet MP, Foster JW. Escherichia coli acid resistance: CAMP receptor protein and a 20 bp cis-acting sequence control pH and stationary phase expression of the gadA and gadBC glutamate decarboxylase genes. Microbiology. 2001;2001(147):709–15.CrossRef
39.
Volkova VV, Lanzas C, Lu Z, Grohn T. Mathematical model of plasmid-mediated resistance to ceftiofur in commensal enteric Escherichia coli of cattle. PLoS ONE. 2012;7(5):36738.CrossRef
40.
Lu P, Ma D, Chen Y, Guo Y, Chen G-Q, Deng H, et al. L-glutamine provides acid resistance for Escherichia coli through enzymatic release of ammonia. Cell Res. 2013;23(5):635–44.CrossRefPubMedPubMedCentral
41.
Seo SW, Kim D, O’Brien EJ, Szubin R, Palsson BO. Decoding genome-wide GadEWX-transcriptional regulatory networks reveals multifaceted cellular responses to acid stress in Escherichia coli. Nat Commun. 2015;6:7970.CrossRefPubMedPubMedCentral
42.
Franchini AG, Egli T. Global gene expression in Escherichia coli K-12 during short-term and long-term adaptation to glucose-limited continuous culture conditions. Microbiology. 2006;152(7):2111–27.CrossRefPubMed
43.
McMahon MA, Xu J, Moore JE, Blair IS, McDowell DA. Environmental stress and antibiotic resistance in food-related pathogens. Appl Environ Microbiol. 2007;73(1):211–7.CrossRefPubMed
44.
Sinel C, Cacaci M, Meignen P, Guérin F, Davies BW, Sanguinetti M, et al. Subinhibitory concentrations of ciprofloxacin enhance antimicrobial resistance and pathogenicity of Enterococcus faecium. Antimicrob Agents Chemother. 2017;61(5):e02763-e2816.CrossRefPubMedPubMedCentral
45.
Olaitan AO, Li J. Emergence of polymyxin resistance in Gram-negative bacteria. Int J Antimicrob Agents. 2016;48(6):581–2.CrossRefPubMed
46.
Srinivas P, Rivard K. Polymyxin resistance in Gram-negative pathogens. Curr Infect Dis Rep. 2017;19:38.CrossRefPubMed
47.
48.
49.
Bolger AM, Lohse M, Usadel B. Trimmomatic: a flexible trimmer for Illumina sequence data. Bioinformatics. 2014;btu170.
50.
51.
Robinson MD, McCarthy DJ, Smyth GK. edgeR: a Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics. 2009;26(1):139–40.CrossRefPubMedPubMedCentral
52.
Mortazavi A, Williams BA, McCue K, Schaeffer L, Wold B. Mapping and quantifying mammalian transcriptomes by RNA-Seq. Nat Meth. 2008;5(7):621–8.CrossRef
53.
Bolstad BM, Irizarry RA, Åstrand M, Speed TP. A comparison of normalization methods for high density oligonucleotide array data based on variance and bias. Bioinformatics. 2003;19(2):185–93.CrossRefPubMed
54.
Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCT method. Methods. 2001;25(4):402–8.CrossRef
55.
Wiegand I, Hilpert K, Hancock REW. Agar and broth dilution methods to determine the minimal inhibitory concentration (MIC) of antimicrobial substances. Nat Protoc. 2008;3(2):163–75.CrossRefPubMed
56.
EUCAST. Recommendations for MIC determination of colistin ( polymyxin E ) As recommended by the joint CLSI-EUCAST Polymyxin Breakpoints Working Group. 2016, p 2016. https://​www.​eucastorg.
57.
Beumer RR, De VJ, Rombouts FM. Campylobacter jejuni non-culturable coccoid cells. Int J Food Microbiol. 1992;15:153–63.CrossRefPubMed
58.
Zhu J, Mekalanos JJ. Quorum sensing-dependent biofilms enhance colonization in Vibrio cholerae. Dev Cell. 2003;5(4):647–56.CrossRefPubMed
Metadata
Title
Transcriptome changes and polymyxin resistance of acid-adapted Escherichia coli O157:H7 ATCC 43889
Authors
Daekeun Hwang
Seung Min Kim
Hyun Jung Kim
Publication date
01-12-2020
Publisher
BioMed Central
Published in
Gut Pathogens / Issue 1/2020
Electronic ISSN: 1757-4749
DOI
https://doi.org/10.1186/s13099-020-00390-5

Other articles of this Issue 1/2020

Gut Pathogens 1/2020 Go to the issue

Letter to the Editor

Fusobacterium nucleatum infection correlates with two types of microsatellite alterations in colorectal cancer and triggers DNA damage

Research

Association of antimicrobial resistance and gut microbiota composition in human and non-human primates at an urban ecotourism site

Research

Molecular characteristics of the VP1 region of enterovirus 71 strains in China

Research

Plasmid mediated colistin resistant mcr-1 and co-existence of OXA-48 among Escherichia coli from clinical and poultry isolates: first report from Nepal

Research

Emergence of plasmid-mediated mcr genes from Gram-negative bacteria at the human-animal interface

Research

The absence of murine cathelicidin-related antimicrobial peptide impacts host responses enhancing Salmonella enterica serovar Typhimurium infection
Obesity Clinical Trial Summary

At a glance: The STEP trials

Read more

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Pediatric Cardiology Video

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

Cardiopulmonary Comorbidity Video

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Valvular Heart Disease Video

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Heart Failure Video

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

ACC 2024 Congress Coverage

Heart Failure Video

Year in Review: Heart failure and cardiomyopathies

Watch now

Watch this official video from ACC.24. Dr. Biykem Bozkurt discuss last year's major advances in heart failure and cardiomyopathies.

Semaglutide benefits people with type 2 diabetes and obesity-related heart failure

16-04-2024 Type 2 Diabetes News

Incentivised to exercise

11-04-2024 Lifestyle Modifications News

New intervention for STEMI-related cardiogenic shock

10-04-2024 Myocardial Infarction News

» View more highlights on the ACC 2024 congress hub page

Image Credits